Evolution of sexual conflict in scorpionflies

  1. Agnieszka Soszyńska-Maj  Is a corresponding author
  2. Ewa Krzemińska  Is a corresponding author
  3. Ricardo Pérez-de la Fuente
  4. Ji-Shen Wang
  5. Krzysztof Szpila
  6. Kornelia Skibińska
  7. Katarzyna Kopeć
  8. Wiesław Krzemiński
  1. Faculty of Biology and Environmental Protection, Department of Invertebrate Zoology and Hydrobiology, University of Łódź, Poland
  2. Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Poland
  3. Oxford University Museum of Natural History, United Kingdom
  4. College of Agriculture and Biological Sciences, Dali University, China
  5. Department of Ecology and Biogeography, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus University, Poland

Abstract

Sexual conflict – opposite reproductive/genetic interests between sexes – can be a significant driver of insect evolution. Scorpionflies (Insecta: Mecoptera) are models in sexual conflict research due to their large variety of mating practices, including coercive behaviour and nuptial gift provisioning. However, the role of palaeontology in sexual conflict studies remains negligible, namely due to the paucity of well-preserved fossils. Here, we describe three male scorpionflies from Cretaceous and Eocene ambers. The structure of notal and postnotal organs is analysed in extant and extinct forms; a depression below the base of the notal organ in different panorpid species spatially matches the anterior fold of the female’s wing. Based on disparate abdominal configurations and correlations in extant relatives, we posit that each new fossil taxon had a different mating approach along a nuptial gifting-coercive spectrum. The Eocene specimen possesses extreme female clamping abdominal armature, suggesting a degree of sexual coercion greater than in any other known scorpionfly, extinct or extant. The fossil record of abdominal modifications in male scorpionflies documents a relatively late evolution (Eocene) of long notal organs indicating oppressive behaviour toward a female during mating. Our findings reveal a wider array of mating-related morphological specialisations among extinct Panorpoidea, likely reflecting more diversified past mating strategies and behaviours in this group, and represent first steps towards gaining a deep-time perspective on the evolution of sexual conflict over mating among insects.

Editor's evaluation

The authors present, describe and interpret exquisite insect fossils preserved in amber. The detailed scorpionfly morphology reveals specific reproductive morphological adaptations that are clear enough to corroborate hypotheses explaining how these insects may have mated. Based on careful morphological comparisons with extant scorpionfly species, the authors are able to speculate on how sexual conflict evolved and shaped insect mating behavior. The findings are of interest to evolutionary biologists studying reproduction and behavior, entomologists and paleontologists. Given the unusual diversity in insect mating behavior, which is simultaneously fascinating and horrifying, this deep-time perspective is likely to interest not only colleagues in the field, but also the general public.

https://doi.org/10.7554/eLife.70508.sa0

Introduction

Sexual conflict between two conspecific sexes arises when divergent interests about the timing and duration of copulation, number of mating partners, or parental investment occur, provided that a trait enhancing the reproductive success (~fitness) of one sex may reduce that of the other (Arnqvist and Rowe, 2005). Currently more broadly defined as the sexually antagonistic selection of shared traits, the sexual conflict is now recognised as a “pervasive evolutionary selective force“, leading in many known instances to a male-female coevolution (Parker, 1979; Rostant et al., 2020). At the very core of this conflict lies the struggle for dominance over genetic control in offspring by each sex (Thornhill, 1976; Thornhill, 1979). The study of mating practices offers one of the most direct ways to address sexual conflict in nature. Two seemingly opposite (yet not necessarily mutually exclusive) mating-related strategies are observed in males: aggressive behaviour toward a female, which allows exerting domination while mating, and the nuptial gifting of food to allure and/or pacify a female during the time of copulation and sperm transfer (Lehmann, 2012; McCartney et al., 2013). Both coercive and nuptial gifting strategies appear costly to males because they are based on the differential allocation of limited resources (Liu et al., 2015); therefore, an exaggerated armature may hinder the overall fitness in a male (e.g. in rhinoceros and flour beetles a larger ‘weapon’ is negatively correlated with wing size; Yamane et al., 2010). In order to incline the female to mate, males show aggression (e.g. calopterygid damselflies; Rivera and Andrés, 2002), intimidating behaviour (e.g. water striders; Han and Jablonski, 2010), and may use special structures, such as modified front legs to clasp the female wings (e.g. sepsid flies; Eberhard, 2002) or adhesive discs to secure grip on the female (e.g. diving beetles; Bergsten et al., 2001). Within coercive mating, extreme cases of aggressive behavior by males, which may cause damage or even death to the female, are known among insects and other invertebrate groups, such as true bugs (Siva-Jothy, 2006), water bugs, and camel-spiders (Arnqvist and Rowe, 2002; Hrušková-Martišová et al., 2010) or snails (Kimura and Chiba, 2015), but also among vertebrates (e.g. ducks; Brennan and Prum, 2012). Nuptial gifting is also widespread. Crickets and bush crickets (Orthoptera: Tettigonidea, Grylloidea) provide an edible gift attached to a structure containing the sperms. Female consume the nutritious part during fertilisation by the spermatozoans, the time for consumption correlating with that of fertilisation (Lehmann, 2012; McCartney et al., 2013). Males of other orthopterans offer thoracic secretions (Gryllidae; Bussière et al., 2005) or even their own hind wings as nuptial gifts (Haglidae; Eggert and Sakaluk, 1994; Sakaluk et al., 2004). Silk-wrapped nuptial gifts of prey are offered by spiders (Stålhandske, 2001) and dance flies (Diptera: Empididae; Preston-Mafham, 1999; Sadowski et al., 1999; Lebas and Hockham, 2005); the shining silk cover makes a gift more enticing and may deceive the female if it only contains a scarce – or even fully absent – edible portion (Ghislandi et al., 2017). In dobson flies (Megaloptera: Corydalidae), the species offering nuptial gifts have a ‘weapon’ armature used for fighting off the rivals smaller than in species whose males rely only (or mostly) on such armature (Liu et al., 2015). Among mecopterans, a gift of prey is offered by hangingflies (Bittacidae; Thornhill, 1976) and scorpionflies (Panorpa spp.; Gwynne, 1984); the latter may offer hardened salivary masses to the female instead (Thornhill, 1979; Bockwinkel and Sauer, 1994). Coercive and nuptial-gifting mating approaches can co-occur in same species, which then exhibits a mixed strategy that can serve as a model to study the trade-off between these two tactics (e.g. Tong and Hua, 2019).

Scorpionflies (Mecoptera: Panorpidae) are models in sexual conflict research. Their mating practices range from coercive to provisioning nuptial gifts, in extreme cases including mouth-to-mouth salivary transfer until the end of copulation (Zhong et al., 2015). Mecoptera are among the oldest holometabolous insects. They are known since the Permian, when they were a significant component of the flying insect fauna. Whereas scorpionflies flourished in the Mesozoic, most of their lineages rapidly declined during the Cenozoic. In fact, mecopterans are considered to have gone through a degree of extinction unparalleled among holometabolans (Grimaldi and Engel, 2005). Extant Mecoptera are classified in nine families, most of which are relict; only two lineages, Panorpidae and Bittacidae, are relatively species-rich. The Panorpidae appeared in the Late Jurassic (Ding et al., 2014) and currently represent the most diverse mecopteran lineage, with about 480 described species classified in seven genera (Bicha, 2018; Miao et al., 2019), that is, c. 67% of extant mecopteran species.

In scorpionfies, the male behaviour towards the female may be coercive in such a degree that the expression ‘rape’ has been used in the past for describing their mating rituals (Thornhill, 1980). In any case, the role of a female in controlling mating and the eventual reproductive outcome appears more active and decisive than initially thought in the group, namely through precopulatory male choice, struggling behaviour to interrupt genital connection, and the selective reception of sperm from gift-providing males (likely through spermathecal muscular action; Kock et al., 2009). The modifications of panorpid males enabling coercive mating behaviour include a diverse array of structures on different abdominal segments as well as thinned and elongate last segments of the abdomen. Some of these structures, the so-called notal and postnotal organs, effectively act as a ‘clamp’, grasping the female’s wing prior to and during the course of copulation (Figure 1A, B, F). Depending on the size and shape of these organs in a species, the grasp is more or less coercive. Elongate abdominal segments enable the males to bend the abdomen over that of the female, while additional, usually paired abdominal structures referred to as anal horns are used to achieve and maintain the strained, twisted copulatory position of both abdomens for the long time required for sperm transmission, which could be more than 3 hr (Tong et al., 2018; Tong and Hua, 2019). Panorpid species with very long notal organs, capable of clamping the entire width of the female wing, only use coercion, so no food gifts are offered (Tong and Hua, 2019). In species with mixed strategies, it is the physical condition of the male which determines the followed strategy (Engqvist and Sauer, 2001): older and weaker males, as well as smaller ones, primarily adopt an aggressive strategy toward a female, as they are either not able to obtain a prey as a gift or to fabricate it through salivary production, or their gift is often been stolen by a stronger male. Larger males also have an advantage over smaller ones when competing for dead arthropods that can be offered to a female or, if eaten by the male, allow to produce salivary masses. On the other hand, conspecific smaller males bear proportionally larger notal organs (Thornhill, 1990), which shows the genetic background of this negative allometry.

Baltipanorpa oppressiva sp. nov. (Panorpidae) from Baltic amber (middle Eocene), holotype MP/2711.

A-B, habitus, photograph of preserved portion (A) and explanatory drawing (B), with genital bulb in ventrolateral view magnified; C-E, notal organ: fully-clasped clamp formed by notal and postnotal organs (C), teeth inside the notal-postnotal clamp (D), detail of terminal clasp (E); F, life reconstruction of entire specimen (head and thorax, missing in this species, based on habitus of congeneric Baltipanorpa damzeni); G, forewing; H, hind wing (same scale in both wings). Abbreviations: Ep, epandrium; HP, horn-like process; Hv, hypovalve; NO, notal process; PO, postnotal process; Gs, gonostylus; Gcx, gonocoxite. Red colour: notal process.

Here, we describe three exceptional scorpionflies from three different Cretaceous and Eocene ambers deposits and each belonging to a distinct panorpoid lineage. The disparate abdominal configurations and specialisations in the new taxa allow us to extrapolate trends observed among extant relatives, discussing possible mating habits for the new fossils and previously described ones with preserved non-genitalic abdominal modifications (Willmann and Novokschonov, 1998; Krzemiński and Soszyńska-Maj, 2012; Archibald, 2013; Wang and Hua, 2020; Zhang et al., 2021). Additionally, the new taxa are of general evolutionary significance, including the description of a new extinct panorpoid family and the first orthophlebiid species described in amber.

Results

Systematic palaeontology

Mecoptera Packard, 1886
Panorpoidea Latreille, 1805
Panorpidae Latreille, 1805

Baltipanorpa Krzemiński and Soszyńska-Maj, 2012

Type species. Baltipanorpa damzeni Krzemiński and Soszyńska-Maj, 2012; Baltic amber.

Other species included. Baltipanorpa oppressiva sp. nov.; Baltic amber.

Baltipanorpa oppressiva Soszyńska-Maj and Krzemiński sp. nov.

(Figure 1A–H)

Zoobank registration: urn:lsid:zoobank.org:act:F95F5F6C-E210-4CCA-9AAA-2AAB51588C78

Etymology. After ‘oppressio’, meaning ‘coercive’ in Latin, referring to the most restraining notal organ ever found within Panorpidae. Gender is feminine.

Material. Holotype MP/2711, most part of the abdomen and wings preserved.

Locality and age. Baltic amber, middle Eocene (ca. 45 Ma).

Diagnosis. Wing membrane with dark maculations (vs. transparent in B. damzeni); notal and postnotal processes very long, reaching end of VII segment, notal process distally forked (vs. notal process shorter than postnotal, and not forked in B. damzeni); abdominal segment V slightly wider than long; tergite V medially bearing large, strongly recurved process (vs. tergite V without process in B. damzeni); segments VII and VIII thinned at base, not particularly elongate, about 3–4× as long as maximal width (vs. segments VII and VIII strongly elongate in B. damzeni).

Description. Body length 7.2 mm as preserved (only abdomen). Head. Antennae partly preserved with 14 cylindrical flagellomeres twice longer than wide. Wings (Figure 1A). Elongate and narrow, almost 3.5× longer than wide, at least 10 mm long, ~ 3 mm wide. Forewing (Figure 1G). Membrane bearing seven maculated areas, largest occupying the wing tip; Sc short and single reaching wing margin in midwing, opposite crossvein m-cu; costal area narrow; R1a and R1b surrounding pterostigmal area; Rs with five branches reaching wing margin, Rs1+2 longer than R3+4; fork of Mb more distal than fork of Rs, crossvein r3+4–m1+2 sinuous; M with four branches reaching wing margin, M1+2 13× longer than M3+4, M4 sharply curved at m-cu; Cu1 and Cu2 fused at base, with two crossveins between them; three anal veins, A1 reaching wing margin proximal to origin of Rs. Hind wing (Figure 1H). Venation very similar to forewing, except for: Mb fused with Cu1, A1 proximally fused with Cu2, only one cu2-a2. Abdomen (Figure 1A and B). Incomplete, longer than wings; first two segments are missing; notal and postnotal processes on tergites III and IV, respectively (Figure 1B), both processes very long (1.2 mm), about equal in length, reaching segment VII; notal process with spine-like setae on inner surface’s distal half (Figure 1B and C), bearing terminal fork curved posteriorly (Figure 1E); postnotal process terminally curved anteriorly, lodged between prongs of notal process (Figure 1B and C), bearing one very long seta at midlength of organ, and few shorter setae in basal part (Figure 1C and D); postnotal organ covered with short and blunt teeth, irregularly distributed on inner surface; tergite V medially bearing a large, strongly recurved process (horn, 300 µm); abdominal segments VI–VIII moderately elongate, with fused tergites and sternites; segments VII–VIII narrower basally. Genitalia (Figure 1B). Genital bulb round; hypovalves narrow, not extending to apex of gonocoxite; gonostylus shorter than gonocoxite.

Orthophlebiidae Handlirsch, 1906

Burmorthophlebia Soszyńska-Maj, Krzemiński and Wang gen. nov.

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Etymology. Combination of Burmo-, after Burmese amber, and –orthophlebia, after the genus Orthophlebia (from the Greek ‘phlebas’, φλέβας, meaning ‘veins’) to emphasize an alleged close relationship to this genus. Gender is feminine.

Type species. Burmorthophlebia multiprocessa sp. nov., by monotypy and present designation.

Diagnosis. Rostrum long and narrow; antenna with at least 30 flagellomeres. Fore- and hind wings with R1 slightly curved in pterostigmal area towards anterior wing margin; Rs with five branches (vs. six and more in other genera of Orthophlebiidae), Rs1+2 and Rs3+4 very long (vs. much shorter in other genera of Orthophlebiidae) Rs1 ascending, Rs1+2 and Rs2 almost at the same level. Forewing with Sc long and simple, reaching pterostigmal area; M with five branches; two crossveins present between M4 and Cu1; two anal veins. Hind wing with Sc single and simple, only reaching M3+4 forking; M with four branches; one anal vein. Abdominal segments VI–VIII moderately elongate; very short notal process on tergite III, not extending beyond end of this tergite; postnotal process absent; two hirsute postnotal areas on tergite IV; tergites VI and VII with a pair of distal appendages each. Genital bulb without stem part, gonostyli long and thin.

Burmorthophlebia multiprocessa Soszyńska-Maj, Krzemiński and Wang sp. nov.

(Figure 2A–H)

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Etymology. Species name highlights the unusual morphology of the holotype, possessing multiple processes on abdominal segments.

Material. Holotype MP/3721, male.

Locality and age. Kachin amber, Myanmar; Late Cretaceous: earliest Cenomanian (98.8 ± 0.62 Ma).

Diagnosis. As for the genus (vide supra).

Description. Body length 9.5 mm from frons to the end of gonostyli (Figure 2A). Head (Figure 2G). Three occipital bristles; rostrum 2 mm long, first five flagellomeres only slightly longer than wide, gradually becoming more elongate, distal visible flagellomeres 3× longer than wide; maxillary palp five segmented, palpomeres slim, ca. 4× longer than wide. Thorax. Legs with setae arranged in whorls, each bearing a pair of long tibial spurs; fifth tarsomere ca. 4× longer than fourth one, two pretarsal claws; first tarsomeres bear no swellings on any leg. Wings. Proximally narrow and significantly broadening distally, 9.5 mm long and ca. 3.5 mm wide; wing membrane bearing a round, dark pigmented spot in medial sector. Forewing (Figure 2C). Sc and R1 reaching pterostigmal area, two crossveins between C and Sc; Rs1+2 almost 3× longer than Rs1, Rs3+4 longer than Rs3 and Rs4; M with five branches reaching wing margin, Mb forking beyond the Rs fork, M1+2 9× longer than M3+4, M4a+b 3.5× longer than M3+4; two m4-cu1 crossveins, the most proximal slightly bending M4; two crossveins between A1 and A2, A3 not visible. Hind wing (Figure 2D) same as in forewing; Mb fused with Cu1; second anal vein reduced or invisible. Abdomen (Figure 2E and F). Elongate, notal organ on abdominal tergite III wide at base and curved toward distal part; postnotal organ on tergite IV composed of two areas of dense brush of short setae (called here postnotal areas 1 and 2), distal part of tergite IV curved upward and covered with dense setation (Figure 2H); abdominal segment V ca. 1/3 longer than wide; segment VI ca. ½ longer (800 µm) than wide, bearing a pair of relatively large anal horns on posterior margin of tergum; distinct sinuous seam between tergites and sternites (Figure 2E and F); tergites and sternites VII–VIII fused; segment VII (1.3 mm) distinctly thinned at base and gradually broadening distally, horns on posterior tergum margin, opposite to them the sternite bears a process with dense setae; segment VIII ca. 2× longer than wide, sternite covered with setae. Genitalia. Genital bulb narrow (Figure 2E); gonostyli longer than gonocoxites, very thin at apex, covered with numerous setae; hypovalve broad; epandrium most likely with two processes.

Burmorthophlebia multiprocessa gen. et sp. nov. (Orthophlebiidae) from Kachin amber, Myanmar (Late Cretaceous), holotype MP/3721.

A, amber piece with habitus in lateral view; B, life reconstruction; C, forewing; D, hind wing, partially reconstructed; E-F, abdomen in lateral view, explanatory drawing (E) and photograph (F); G, detail of head in lateral view, antennae and rostrum; H, notal process and postnotal areas (on tergites III and IV, respectively). Abbreviations: AH, anal horns; PA1, PA2, postnotal areas 1, 2; other symbols as in Figure 1.

Remarks. Burmorthophlebia gen. nov. differs from all other genera of the family Orthophlebiidae in number of veins in radial sector, and in unusually long veins Rs1+2 and Rs3+4 which are only terminally forked, at level of end of Sc. Wings of Burmorthophlebia gen. nov. are more narrow than in other orthophlebids. Five veins in radial sector are present also in a recently established family Protorthophlebiidae (Soszyńska-Maj et al., 2019), but the rostrum in this family is short (only c. twice as long as its maximum width), and VI-VIII abdominal segments in male are shorter than wide, while Burmorthophlebia gen. nov. has a long rostrum and elongate abdominal segments, both characters typical to orthoplebids.

Cantabridae Soszyńska-Maj, Pérez-de la Fuente, Krzemiński and Wang fam. nov.

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Type genus Cantabra gen. nov., by monotypy and present designation.

Diagnosis. Head with three pairs of long ocellar bristles, rostrum elongate; pronotum elongate, longer than head, bearing long bristles; Sc single, costal area narrow, R and M sectors with four branches in both wings, crossvein cu2-a2 present in hind wings; male abdomen much longer than wings, with elongate and narrow segments VI–VIII, tergites and sternites VII and VIII fused; male gonostylus without median tooth, with several minute denticles.

Remarks. The wing venation and general habitus of Cantabra gen. et. sp. nov. resemble those of the Panorpidae and Panorpodidae. The new fossil species differs from panorpids in the distinct body bristles, particularly those on head and thorax, an unusually elongate pronotum, clearly longer than the head (shorter in panorpids), and the lack of median tooth on the inner surface of male gonostyli, instead bearing several minute denticles in a row. From panorpodids, Cantabra gen. et. sp. nov. differs in greatly elongate rostrum, elongate abdomen and fused VII and VIII abdominal segments. The remarkably elongate and narrow male abdomen of the new taxon resembles extinct family Holcorpidae, but differs from the latter in five veins in medial sector in both wings and less elongate abdominal segments VI-VIII (Archibald, 2013).

Cantabra Soszyńska-Maj, Pérez-de la Fuente, Krzemiński and Wang gen. nov.

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Type species. Cantabra soplao sp. nov., by monotypy and present designation.

Etymology. After the Latin ‘cantabra’ (‘cantabrum’ in neutrum) meaning ‘from, or pertaining to, Cantabria’ – that is, the Autonomous Community of Spain where the El Soplao outcrop is located. Gender is feminine.

Diagnosis. As for the family (vide supra).

Cantabra soplao Soszyńska-Maj, Pérez-de la Fuente, Krzemiński and Wang sp. nov.

(Figures 3A–G and Figures 4A–E)

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Etymology. After the El Soplao amber outcrop, where the amber inclusion was found. The specific epithet is treated as a noun in apposition.

Material. Holotype CES-437, male.

Locality and age. El Soplao amber outcrop; middle Albian, Early Cretaceous (ca. 105 Ma).

Diagnosis. As for the genus (vide supra).

Description. Body length ~9.25 mm without antennae (Figure 3A). Head (Figure 3B and C). Rostrum with preserved proximal part about 1.5× as long as that of head; 20 flagellomeres preserved, all elongate, 2–3× as long as wide, covered with microsetae; three pairs ocellar bristles on vertex, ~ 350 µm long, probably surrounding ocelli (the latter not discernible). Thorax. Pronotum with long bristles, ~ 300–350 µm long; only one right foreleg partially preserved, elongate, rather delicate, bearing microsetae on its entire length; femur bearing ventral bristles; tibiae with a few whorls of spike-like setae arranged in whorls and bearing two long spurs distally. Wings. Only right wings fully preserved. Wings elongate and narrow, almost 4× longer than wide, 6.5 mm long, 1.7 mm wide; C covered with setae, longer and thinner in anal region. Forewing (Figure 4A). Costal area narrow, with Sc unbranched and long, reaching wing margin opposite tip of M4; R1 faint, its two branches surrounding pterostigmal area; radial sector with four branches; Rs1+2 almost twice as long as Rs3+4; M1+2 almost 7× longer than M3+4; Cu1 and Cu2 fused at base; three anal veins present, A1 reaching the wing margin beyond fork of Rs; short spines along anal veins and wing membrane on anal area; jugal area with few long bristles. Hind wing (Figure 4B). Venation mostly similar to that of forewing, except short Sc, not reaching beyond the level of end of Cu1; R1 forking at the level of end of Cu1; Mb fused with Cu1; A1 proximally fused with Cu2 and reaching wing margin only slightly beyond fork of Rs; one crossvein between Cu2 and A2; crossveins hardly visible. Abdomen (Figure 4C). Significantly longer than wings; tergite III not visible dorsally, notal organ not discernible, but (if present) not long, (otherwise it would be visible above tergite IV); small postnotal organ present on tergite IV; long bristles on sternites IV–V; abdominal segments VI to VIII elongate and narrow, segment VI (1.8 mm long) 7× longer than wide, segment VII (1.4 mm) 6× longer than wide, segment VIII (1.5 mm) 10× longer than wide; segment VI most probably with a fusing seam; segments VII and VIII with tergites and sternites fused. Genitalia (Figures 3F, G, 4C, D). Genital bulb elongate, hypovalves probably broad, not extending to apex of gonocoxites; gonostyli (1 mm) longer than gonocoxites (700 µm), slender, inwardly curved at apex, without median tooth, and with rounded and relatively small basal processes; inner margin of gonostylus with at least eight short triangular denticles in a row along median and basal parts; basal processes of parameres long and curved ventrally, with their basal branch rounded, covered with dense microsetae reaching apex of gonocoxite.

Photomicrographs of Cantabra soplao gen.

et sp. nov. (Cantabridae fam. nov.), from El Soplao amber, Spain (Early Cretaceous), holotype CES-437. A, ventral and lateral habitus, respectively; B-C, head, frontoventral view (B), lateral view (C); D, setae on anal area of forewing; E, postnotal organ seen in ventrolateral view (head is to the left), morphology distorted due to the skewed view; F, genital bulb in ventral view; G, detail of gonostylus, showing its inner denticles. Abbreviations: OB, ocellar bristles; PO, postnotal organ.

Explanatory drawings of Cantabra soplao gen.

et sp. nov. (Cantabridae fam. nov.) from El Soplao amber, Spain (Early Cretaceous), holotype CES-437. A, right forewing; B, right hind wing (same scale for both wings); C-D, reconstruction of abdomen in lateral view, with genital bulb shown in ventral view (C); inset (arrow) shows the genital bulb expanded, with elements tagged (D); E, life reconstruction, in resting position. Notal organ not visible in holotype and thus not depicted for caution. Length of antennae and rostrum are conjectural; morphology of legs is based on the preserved left foreleg, which is mostly complete. Abbreviations: Bp, basal process; Pm, parameres; other symbols as in Figure 1.

Discussion

A series of clamping devices used to seize and hold different body parts of the female during courtship and copulation exist in panorpid males. These structures ensure the eventual genital connection and sperm transfer and extend copulation time (Zhong and Hua, 2013a; Zhong et al., 2014). The latter is critical for males, as the more prolonged the copulation, the more sperm can be transferred and, thus, the greater the number of potentially fertilised eggs (Engqvist and Sauer, 2002; Kullmann and Sauer, 2005). Aside from genital clamping structures (among which the most conspicuous is a pair of pincer-like gonostyli), panorpids present non-genital clamping systems on their abdomens. These are notal and postnotal organs, as well as anal horns which are used to catch and immobilize female during mating. Based on the size, shape and interlocking mechanism of these clamping structures, the grasp on the body of female becomes more or less secure, therefore facilitating a greater degree of coercion during mating, which has been associated with less investment in costly nuptial gifts (Tong and Hua, 2019).

Notal and postnotal organs

The notal organ (NO) is a process on abdominal tergite III. The postnotal organ (PO) typically consists of a small process on abdominal tergite IV (Crampton, 1931; Mickoleit, 1971). In extant scorpionflies, both structures are present in most Panorpidae, the only recent species from the Eomeropidae (the ‘living fossil’ Notiothauma reedi MacLachlan, 1877 [MacLachlan, 1877; Crampton, 1931]), and can be vestigial, if present, in the Panorpodidae (Tong et al., 2017; Wang and Hua, 2018a). Both NOs and POs act jointly by typically creating a clamping structure that grasps the female forewing before and during copulation; in panorpids, these organs allow to achieve and maintain the typical V-shaped mating position (Figure 6A and B; Byers and Thornhill, 1983). Moreover, the NO and the PO bear specialised setae, cephalically directed and thinned terminally, which interlace and/or electrostatically interact with both venational setae and membrane microtrichia from the female’s wing (Zhong and Hua, 2013a). Observations on three species of Neopanorpa van der Weele, 1909 (van der Weele, 1909) bearing NOs of different lengths have shown different mating strategies in these species (Zhong and Hua, 2013a; Tong and Hua, 2019). Males of two species with short and medium-sized NO, i.e. N. lui Chou and Ran, 1981 (Chou et al., 1981) and N. carpenteri (Cheng, 1957) indirectly transfer a nuptial gift of a salivary secretion prior to copulation. The short NO of N. lui ends at the base of the PO, and the medium sized NO in N. carpenteri reaches the end of the abdominal segment IV; both stabilize the female wings only partially and apparently play an auxiliary role during copulation. Contrarily, N. longiprocessa (Hua and Chou, 1997), with a long NO capable to cover the entire wing width of the female, exclusively relies on coercive copulation, and does not offer nuptial gifts. Short NOs and POs pinch only the anterior margin of female forewings, and both processes are spatially suited to fit the latter. In Panorpa amurensis MacLachlan, 1872 (MacLachlan, 1872) (Figure 5A,B), the space created by the clasped NO and PO matches the space of the anterior valley fold of the female wing delimited by the convex costal vein (C), the concave subcostal vein (Sc), and the convex radial vein (R1), clamping together with the PO before or at the latter vein. Our measurements of these distances in this and other panorpid species with various NOs indicate that this seems to be an effective arrangement to grip the anterior wing fold of the female (see Supplementary file 1 for measurements). As the C, Sc, and R1 run almost parallel over a long stretch, the female forewing may be gripped more anteriorly or posteriorly, usually by its half or basal third, as can be observed in photographs of mating panorpids (Zhong and Hua, 2013a; Zhong et al., 2014; Tong and Hua, 2019).

Spatial coupling between short male notal organs and female (fore)wings during mating in extant and extinct Mecoptera.

A–B, Panorpa amurensis MacLachlan, 1872 (Recent): A, photograph of notal organ in male, and diagram cross-section through the notal and postnotal processes with anterior fold of female forewing entrapped; B, photograph and diagram of anterior fold in female forewing; C-D, Orthophlebia heidemariae Willmann and Novokschonov, 1998 (Late Jurassic): habitus (C) and explanatory drawing (D, inset showing notal-postnotal system magnified); E, Burmorthophlebia multiprocessa, gen. et sp. nov (Late Cretaceous): diagram of abdominal modifications (bottom) and hypothetical spatial coupling between male notal organ and female wing (top). Abbreviations: SP, small process (tergite VII); other as in Figures 1 and 2. Colour legend of cross section through veins: black circle, C (Costa); blue circle, Sc (Subcosta); red circle, R1 (1st radial vein); red line, wing membrane.

A short NO of the type similar to that in Recent panorpids was already present among the Late Jurassic panorpoids, as evidenced by Orthophlebia heidemariae (Willmann and Novokschonov, 1998; Figure 5C, D). This species is currently classified in Orthophlebiidae, a Mesozoic polyphyletic panorpoid assemblage ancestral to Panorpidae (Soszyńska-Maj et al., 2019). In Burmorthophlebia multiprocessa gen. et sp. nov. the NO, although also short, differs from all the hitherto known in Mecoptera, extinct or extant. The NO is distinctly raised over abdomen but poorly pronounced, not reaching any process to form a clamp with. The PO is here replaced by two elevated areas on tergite IV, the postnotal areas 1 and 2 (PA1 and PA2; Figure 5E). The former is mound-like, located after an anterior depression on tergite IV and at a distance from the NO comparable to that of C to R1. The PA2 is sharply elevated, and measurements show that it contacted the female wing just at or slightly beyond the concave radial sector vein (Rs). Both PAs were involved in adhering the female’s wing as indicated by their location and specialised setation, consisting of short and dense tufts of hairs different from other abdominal bristles. Apparently, only the costal vein and a brief anterior wing membrane portion were covered by the NO in B. multiprocessa gen. et sp. nov., and so the remaining portion of the female wing was to a certain degree immobilised by the setation of both PAs. Among the extant panorpids the hirsute PAs, more flattened than those of Burmorthophlebia gen. et sp. nov. and situated on three consecutive tergites, have been described in Neopanorpa setigera Wang and Hua, 2018 (Wang and Hua, 2018b) and N. luojishana Wang and Hua, 2019 (Wang and Hua, 2019b), and also exist in N. longistipitata Wang and Hua, 2018 (Wang and Hua, 2018b). However, in these species the NO is long and able to keep the entire wing of a female pressed against the male’s abdomen to a lesser or greater extent, so the hirsute PAs are probably only of auxiliary importance (Figure 6A–D). This contrasts with the armature in B. multiprocessa gen. et sp. nov., where it was the interaction between NO-PO setae and the integumentary structures of the female’s wing that kept a larger portion of the latter in place, although the fixing must have been weaker. Recent panorpids with a short NO (and anal horns) adopt a mixed mating strategy (Neff and Svensson, 2013). After a courtship ritual, males present nuptial gifts to the female, but if they are not able to get one ready (including if they have been stolen by other males) or the gift is deemed as unsatisfactory by the female (e.g. small salivary secretions due to poor condition of the male), they resort to attempt coercive copulation (Thornhill and Sauer, 1991). Burmorthophlebia multiprocessa gen. et sp. nov., with its short NO and no other armature to immobilize the female’s wing, probably had a similar approach when mating.

Spatial coupling between long male notal organs and female (fore)wings during mating in extant and extinct Mecoptera.

A–D, Neopanorpa longistipitata Wang and Hua, 2018 (Recent): A, photograph of mating couple; inset (arrow) shows notal and hypovalves connection magnified; B, diagram of mating couple (notal organ depicted in red); C, photograph of male abdomen in lateral view; D, diagram of coupling mechanism between male notal organ and genital bulb; E, F, spatial coupling diagram between male notal-postnotal clip clasping the female wing in two species of Baltipanorpa (Eocene): B. damzeni Krzemiński and Soszyńska-Maj, 2012 (E); B. oppressiva sp. nov. (F). Abbreviations as in Figures 1, 2, 4 and 5.

As introduced above, long NOs differ mechanically from short NOs. They are present in a small group of species classified in the genera Panorpa and Neopanorpa (Hu et al., 2015; Tong and Hua, 2019; Wang and Hua, 2018a). Instead of a pincer-like clamp composed by a PO and NO, the long NO covers the entire female’s wing across its full width and immobilizes it more or less pressed against the abdomen. As the mating couple of N. longistipitata shows (Figure 6A–D), the leading edge of the female wing is also accommodated in a small depression of tergite IV under the base of the NO. As can be deduced from measured distances, of the three hirsute PAs on tergites IV–VI the first one supports the wing fold by the convex R1; the more distal part of the wing is pressed against the abdomen by the long NO with the help of special muscles (Thornhill, 1990). The tip of the NO is locked between the genital hypovalves. Although this conformation fully encloses the female wing during mating, the resulting grip is likely not particularly tight. In any case, nuptial gifts are not offered prior or during the mating of Neopanorpa species with a long NO, such as N. longiprocessa (Zhong and Hua, 2013a), which would suggest that such process enables highly coercive mating behaviour.

Among extinct mecopterans, an extremely long NO was hitherto only known in Baltipanorpa damzeni from Baltic amber (Krzemiński and Soszyńska-Maj, 2012). In this species, the NO forms together with an unusually elongate PO a clip-like structure able to reach beyond the full width of the female’s wing during mating (Figure 6E). Both NO and PO possess short tooth-like bristles, which would have increased their holding power. The PO is bent anteriorly, partially securing the clip in this way. Baltipanorpa oppressiva sp. nov has a similarly characteristic NO-PO clip bearing inner tooth-like bristles, but its NO is terminally forked in two prongs bent posteriorly at an almost right angle, which embrace the tip of PO (Figures 1B, E, 6F). The interaction of these structures in the new species results in a full clasp-like mechanism. The female wing enclosed in this remarkable clamp was likely fully immobilised, a withdrawal attempt probably causing risk of tearing the wing membrane. A similar function, although less effective than that in B. oppressiva sp. nov, must have been accomplished in B. damzeni by a few pairs of elongate bristles on the posterior side of the NO (Figure 6E). Furthermore, the NO-PO clamp in Baltipanorpa is raised at angle of about 50° from the abdomen, and so the captured female’s forewing was also kept raised and separated from the male’s abdomen. This position is deemed as genuine (not preservational) as it is now known from two different species (Figure 6E and F) and is unique to this genus. In extant panorpids with very long NOs (Neopanorpa), this process is placed at a much lower angle and keeps the female wing rather flat against the abdomen, having no other counterpart such as the long PO in the two fossil Baltipanorpa species discussed herein (Figure 6A and D).

Anal horns

The anal horns are distal processes directed posteriorly on abdominal tergite VI. Among extant panorpids, anal horns are single (in Cerapanorpa Gao, Ma and Hua, 2016 (in Gao and Hua, 2016), Megapanorpa Wang and Hua, 2018 (Wang and Hua, 2018a), and some species of Panorpa Linnaeus, 1758), or paired Dicerapanorpa Zhong and Hua 2013 (Zhong and Hua, 2013b), and arise at different angles from the dorsal end of tergite VI (Zhong et al., 2014; Tong et al., 2018; Wang and Hua, 2019a). Aside from panorpids, anal horns are also known in Notiothauma reedi (Eomeropidae; Crampton, 1931; Mickoleit, 1971). In conjunction with tergite VII, which is proximally narrowed and/or depressed, the anal horns create a clamping system to accommodate and hold the female’s terminal abdomen into the strained copulatory position necessary for sperm transmission. It has been demonstrated that anal horns play an important role at initiating copulation and in prolonging its duration in the absence of nuptial gifts and under female resistance, and that the lack of anal horns is correlated with the inability to prolong copulation after gift provisioning (Zhong et al., 2014).

Burmorthophlebia multiprocessa gen et sp. nov. bears a pair of anal horns raised at a 45° angle (Figures 2E, F, 5E). By comparison with extant species, these processes must have been involved in manipulating and holding the female abdomen during mating. Paired anal horns in other fossil species are known in Orthophlebia longicauda Willmann and Novokschonov, 1998 (Orthophlebiidae; Late Jurassic of Karatau in Kazakhstan) and in two species of Holcorpa Scudder, 1878 (Holcorpidae) from two Eocene localities (Florissant, Colorado, USA, and the Okanagan Highlands, British Columbia, Canada) (Scudder, 1878, Willmann and Novokschonov, 1998; Archibald, 2013).

Other mating-related modifications in males

Aside from notal-postnotal organs and anal horns, other male abdominal processes involved in the physical interaction with the female during mating are occasionally present in scorpionflies. Among extant panorpids these are positioned on the ventral side, such as a long process on abdominal sternite III (Neopanorpa furcata (Hardwicke, 1823)) and a ‘ventral hook’ on sternite VI (Leptopanorpa linyejiei Wang and Hua, 2020) (Hardwicke, 1823; Wang and Hua, 2020). In fossil panorpoids, other male abdominal structures with assumed clamping function occurred in the Late Jurassic species Orthophlebia heidemariae. This was the case of a large medial horn-like process on tergite V (Figure 5C and D). Such process has been referred to as ‘tergal spine’, ‘unpaired median tergal process (monocornus)’, or a ‘median tergal horn’ (Crampton, 1931; Mickoleit, 1971; Willmann and Novokschonov, 1998, respectively). It is probable that this process was also used to fix the female abdomen during mating in conjunction with other more distal structures from the male dorsal abdomen. The abdomen of O. heidemariae is preserved in an upturned position and forming a full circle (Figure 5C), which is a frequent mating position among panorpid males. The large horn-like process is opposite to a small putative process and notch on tergite VII (Figure 5D); both structures likely interlocked with one another to facilitate a strained copulatory position (Willmann and Novokschonov, 1998). In Baltipanorpa oppressiva sp. nov. the horn-like process on tergite V is strongly recurved, and the subsequent tergite VI has an anterior depression and a greatly expanded end, resulting in a notched shape. Both specialised shapes strongly suggest that this horn and the tergite VI were engaged in holding the female abdomen during mating (Figure 6F). Such conformation was enabled to a certain extent by the position of the female’s wings (at least a forewing) which was raised high (56°) over the male’s abdomen and secured in this position by the extremely long notal-postnotal clip unique to Baltipanorpa. Moreover, Burmorthophlebia multiprocessa gen. et sp. nov. bears paired processes directed posteriorly at 45° angle on tergite VII, similar to the paired anal horns present on tergite VI, but smaller. Alleged homologous structures have been formerly referred to as ‘paired tergal processes (bicornua)’ or ‘lateral tergal horns’ (Crampton, 1931; Mickoleit, 1971). The most plausible function for these processes in this new species was also holding the female terminal abdomen during mating.

Cantabra soplao gen et sp. nov. has greatly elongate abdominal segments VI–VIII. Among extant panorpids, such development is present in species of Leptopanorpa MacLachlan, 1875 (MacLachlan, 1875) endemic to Indonesia, and also in a few Neopanorpa species (Wang and Hua, 2020). Although biology of these taxa remains unknown, the greatly elongate abdomens are considered to be influenced by sexual selection, in displays to females and competition among male rivals. Extremely elongate abdomens were also present among other extinct panorpoid lineages: the Orthophlebiidae (Willmann and Novokschonov, 1998), the Holcorpidae (Archibald, 2013; Li et al., 2017; Zhang et al., 2021), and in taxa of uncertain relationships from the Middle Jurassic of China, where abdomen elongation was extreme (Wang et al., 2013). Great abdominal elongation is regarded as a result of convergence (Wang and Hua, 2020). Additionally, in the Holcorpidae and Orthophlebiidae swellings on the first tarsomeres of the hind legs in males were most probably used in sexual display; the size and shape of these swellings was likely species specific (Zhang et al., 2021). In the mecopterans presented herein the tarsomeres were not modified (yet in Cantabra soplao gen. et sp. nov. the shape of legs is unknown). Tarsal swellings do not occur in Recent Panorpoidea.

Conclusions

The morphology of the male’s abdomen in extant scorpionflies represents a good approximation to the mating strategy used toward a female. Thus, the abdominal structures of fossil specimens have the ability to convey information on the likely reproductive strategies of extinct scorpionflies and, to some extent, on their evolution. Based on the disparate male abdominal shapes of the three fossil taxa described herein, these almost certainly had different mating strategies along a nuptial gifting-coercive gradient as observed among their extant panorpid relatives. Firstly, the Cretaceous species Cantabra soplao gen. et sp. nov., currently the only known member of its lineage, bears a small PO, with the absence of other posterior abdominal processes. This suggests that its mating behaviour was devoid of coercion and that nuptial gifting must have played an important role in these scorpionflies. Extant panorpid species which NO-PO system is very small or even absent and lack posterior abdominal processes (‘horns’) either rely on nuptial edible gifts or on mouth-to-mouth feeding during copulation adopting an O-shaped position instead of the typical V-position (Figure 6A; Zhong et al., 2015). It is plausible that the mating in C. soplao gen. et sp. nov. was similar. Regardless, the great degree of elongation of the abdomen in this species was probably involved in sexual selection dynamics.

Secondly, the Cretaceous Burmorthophlebia multiprocessa gen. et sp. nov., the only orthophlebiid specimen described from amber to date, likely exhibited a mixed mating strategy involving both nuptial gifting and coercive behaviour, as observed in some extant Panorpidae species. This inference is based on a weak notal-postnotal clamping system and two sets of paired processes on the abdomen, which likely ensured female restraint and probably extended copulation beyond any possible nuptial gift stages. Noteworthy, abdominal processes are exceptionally abundant in this species, on the dorsal and ventral sides. Such armature is unknown among extant Panorpidae, and can be compared only with that of Nothiotrauma reedi of the relict family Eomeropidae.

Lastly, in the Eocene Baltipanorpa oppressiva sp. nov. the NO-PO wing clamp, which resembled a sealing clip, was able to tightly grasp the full wing width of the female. Unlike its previously known congeneric relative B. damzeni, this structure bore a sophisticated terminal clasp. Together with a highly recurved abdominal horn in this new species, these traits represent the most extreme set of female clamping devices known among scorpionflies, both extinct or extant. Consequently, a fully coercive mating strategy was likely dominant, even exclusive, in this species. During copulation, the female wings (at least the forewings) were likely kept in the notal-postnotal clamp well raised over the male abdomen, this way being separated from the male’s anal horn, which is positioned more proximally in this species (i.e. on tergite V vs. in tergite VI in other panorpids). This inclined position of the female’s wing(s) enabled the entrapment of her abdomen by the male’s anal horn during mating. In evolutionary terms, the fitness costs of such organs and the resulting coercive mating behaviour might have been too high for Baltipanorpa. The very long notal and postnotal processes (Figure 6E and F) raised over the male’s body might have hindered flight ability; moreover, because of their size (and perhaps their permanently raised position) these processes were likely prone to injury and thus they might entail a risk for their bearers. These factors might have contributed to the extinction of Baltipanorpa and its singular morphology, so that the evolution of this extreme clamping device resulted in a blind alley. Moreover, the biology of the female could have also contributed to this extinction if the mating became too oppressive or dangerous, related to the risk of tearing the wing membrane with the teeth and hard bristles of the male’s notal organ.

The remarkable diversity of abdominal configurations shown herein suggests that panorpoid mecopterans had accordingly disparate mating strategies and behaviours in the past. Data based on fossil and extant species suggest that the coercive mating behaviour in this group is secondary (derived) from the habit of nuptial gifting. According to the current fossil record, long notal organs did not evolve prior to the Eocene (Figure 7; Supplementary file 2). Data from extant mecopterans point at the Choristidae as the sister group of Panorpoidea (Willmann, 1989; Wang and Hua, 2021), which lack notal organs or other abdominal modifications (including elongate distal segments) and adopt an O-shaped mating position while the male transfers mouth-to mouth salivary secretion to the female (Zhong et al., 2015). Hence, it is assumed that the latter condition is likely plesiotypic for Panorpoidea.

Male abdominal modifications in extinct and extant Panorpoidea on a time scale: A, Orthophlebia heidemariae Willmann and Novokschonov, 1998 (Orthophlebiidae); B, Cantabra soplao gen et sp.

nov. (Cantabridae fam. nov.); C, Burmorthophlebia multiprocessa gen. et sp. nov. (Orthophlebiidae); D. Baltipanorpa damzeni Krzemiński and Soszyńska-Maj, 2012 (Panorpidae); E, Baltipanorpa oppressiva sp. nov. (Panorpidae); F-I, some examples of extant Panorpidae species: F, Leptopanorpa linyejiei Wang and Hua, 2018; G, Leptopanorpa jacobsoni van der Weele, 1909; H. Neopanorpa longistipitata Wang and Hua, 2018; I. Panorpa jinhuaensis Wang and Hua, 2019. Notal processes depicted in red. Drawings not at same scale.

Our data provide first steps toward gaining a deep-time perspective able to inform discussions on the evolution of mating-related sexual conflict in Mecoptera and in insects more generally. Extant fauna show that extreme female holding mechanisms such as those from Baltipanorpa did not survive until today among scorpionflies (Wang, 2020). In fact, mating strategies involving gift provisioning appear to have been evolutionarily favored among mecopterans contrary to forced mating, and likely more prone to promote the species' genetic diversity. In order to start formulating hypotheses about when mating strategies –including those fully coercive– and associated anatomical structures of scorpionflies appeared throughout evolutionary history, it will be necessary to keep discovering fossil males with good abdominal preservation. The latter will in turn necessitate from improving the knowledge on the currently contentious phylogenetic relationships among mecopteran groups.

Materials and methods

Geological context

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The geographical provenance of the amber samples used in this study is marked on the map provided (Figure 8). The Spanish amber sample was gathered in official excavations with the participation of one of us (RPF) taking place between 2008 and 2010 in the El Soplao outcrop (near Rábago village, Cantabria, northern Spain) (Najarro et al., 2009; Najarro et al., 2010), and is dated as middle Albian, Early Cretaceous (ca. 105 Ma) (Barrón, pers. comm.). The Myanmar amber sample comes from Kachin, near Tanai town, Hukawng Valley, Kachin State, Myanmar, and is dated as earliest Cenomanian (98.8 ± 0.62 Ma), Late Cretaceous (Shi et al., 2012). It was acquired in 2016, prior to the armed conflict and the escalation of the ethnic strife in the area (Haug et al., 2020; Szwedo et al., 2020). The age of Baltic amber is estimated as Lutetian, middle Eocene (ca. 45 Ma) (Grimaldi and Ross, 2017), or as late Eocene (Kasiński et al., 2020).

Geographical provenance of amber specimens studied herein.

The two white stars represent Cretaceous localities (El Soplao amber, Spain; Kachin amber, Myanmar); the yellow star an Eocene deposit (Baltic amber).

Specimen repository

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All the studied specimens are deposited in public institutions. Holotype CES-437 is deposited at the Institutional Collection from the El Soplao Cave (Government of Cantabria), Celis, Cantabria, N Spain. The specimen is partly preserved, the amber piece was polished and included in Epoxy resin for visibility and protection. Holotype MP/3721 is housed at the collection from the Museum of the Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland (ISEA PAS). The specimen is almost complete, several cracks cut the specimen. Holotype MP/2711 is housed at the collection of the Museum of the ISEA PAS, Kraków, Poland. The specimen is well preserved but incomplete, a neuropteran and a cecidomyiid dipteran are present as syninclusions.

Methods

Photographs of amber inclusions were taken with a Leica M205C stereomicroscope and an attached Leica DFC295 camera, under a Nikon Eclipse E100 compound microscope with an attached Nikon DS F11 camera at the University of Łódź, and with a Nikon SMZ25 stereomicroscope equipped with a Nikon DS-Ri2 digital camera at the ISEA (PAS). In most instances, incident and transmitted light were used simultaneously. Stacks of photographs were processed using NIS-Elements Imaging Software. Drawings were obtained based on the photographs but corroborating the morphological details under the optic equipment, and then digitally processed in CorelDraw X10.

Adult extant scorpionflies were caught by one of us (JSW) with a collecting net and then preserved in 95% ethanol or pinned. These specimens are deposited at the Biological Science Museum, Dali University (DALU), Yunnan Province, China. Photographs of the insects were taken with a Nikon D7000 digital camera with a Nikkor AF-S Micro 105 mm f/2.8 lens. The figured specimens of Panorpa amurensis were collected by Sigitas Podenas in South Korea in 2014, and are deposited at the collection of the Department of the Invertebrate Zoology and Hydrobiology, University of Łódź, Poland.

Maps were built using the app Maps-For-Free (https://maps-for-free.com) and modified with the software programs Corel Draw and Corel Photopaint X7.

Wing venation terminology follows that of Tillyard, 1933, with minor modifications after Soszyńska-Maj et al., 2018. Wing vein abbreviations: A, anal vein; C, costal vein; Cu, cubital vein, M, medial vein; R, radial vein; R1, first radial vein; Rs, radial sector vein; Sc, subcostal vein. Other abbreviations used in figures appear in their respective captions.

This published work and the associated nomenclatural acts have been registered in ZooBank, the online registration system for the International Code of Zoological Nomenclature. The ZooBank LSIDs (LifeScience Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix “http://zoobank.org/”. The LSID for this publication is urn:lsid:zoobank.org:pub:391453EC-D289-41A6-9C62-C3A78617D012.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the supplementary materials. Additional information related to this paper may be requested from the authors. Investigated fossils are available in public institutions: at the Institutional Collection from the El Soplao Cave (Government of Cantabria), Celis, Cantabria, N Spain and at the collection from the Museum of the Institute of Systematics and Evolution of Animals (ISEA), Polish Academy of Sciences (PAS), Kraków, Poland.

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    In: Bekoff M, Jamieson D, editors. Adaptation Interpretation and Explanation in the Study of Behaviour. Boulder: Westview Press. pp. 1–466.
    1. Tillyard RJ
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    The Panorpoid Complex in the British Rhaetic and Lias
    Britain Museum Fossil Insects 3:1–79.
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    Mecoptera and Planipennia of lnsulinde
    Notes from the Leyden Museum 31:1–100.
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    Zhengzhou: Henan Science and Technology Press.
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    Phylogeny and Taxonomy of the World Panorpidae (Mecoptera). Dissertation
    Shaanxi, China: College of Plant Protection Northwest A&F University.
    1. Willmann R
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    Evolution und phylogenetisches System der Mecoptera
    Abhandlungen Der Senckenberg Gesellschaft Für Naturforschung 544:1–153.

Decision letter

  1. David Lentink
    Reviewing Editor; University of Groningen, Netherlands
  2. Molly Przeworski
    Senior Editor; Columbia University, United States
  3. Ren Dong
    Reviewer
  4. Alexei Bashkuev
    Reviewer
  5. Dany Azar
    Reviewer

In the interests of transparency, eLife publishes the most substantive revision requests and the accompanying author responses.

Decision letter after peer review:

Thank you for submitting your article "Evolution of sexual conflict in scorpionflies" for consideration by eLife. Your article has been reviewed by 4 peer reviewers, and the evaluation has been overseen by a Reviewing Editor and Molly Przeworski as the Senior Editor. The following individuals involved in review of your submission have agreed to reveal their identity: Ren Dong (Reviewer #1); Alexei Bashkuev (Reviewer #2); Dany Azar (Reviewer #3).

The reviewers have discussed their reviews with one another, and the Reviewing Editor has drafted this to help you prepare a revised submission. Please comply with the comments and suggestions to your best ability, mark all changes using a blue font to indicate changes in the revised manuscript, and respond in a point-by-point fashion. This is essential to enable the reviewing editor to fully evaluate the merit of your revision.

Essential revisions:

General points

The following revisions improve both the scientific presentation and clarity for eLife's broad readership. Especially considering the paper has strengths in its unique fossil data, however, there is a need to more clearly and logically support the main points informed by the data. Several sections are unnecessary complex, which makes this manuscript unclear for both specialists and general eLife readers alike. Please address the issues thoughtfully and holistically keeping in mind eLife serves the entire biology community by publishing exceptionally clear and rigorously supported manuscripts. Any jargon deemed essential in the manuscript should be introduced in a more accessible fashion upon first use so a general reader can follow.

1) Not only the general readership needs improved higher level framing to enable a clear read. Fellow paleoentomologists would also greatly benefit from a paragraph in the introduction that includes other insects that follow similar strategies (e.g. Tettigoniidae, Megaloptera) together with some of the most relevant and general references. Considering the species found in Spanish amber belong to a new family, it will be challenging to make comparisons with recent relatives. Hence it may serve both the general and specialist reader to present the current findings in the context of mating strategies of other insects with sexual conflicts. To help introduce the general reader to the focus of this study, it would help to present an introductory figure showing this broader context, both in extant and extinct species, highlighting the unique contribution the new fossils make. Optimizing the graphic presentation and introducing key specialist terms in a clear fashion. To find examples for what a general reader would find clear consider how an in-depth National Geographic or New York Times Science article would communicate the context of the new finding and fossil as inspiration for designing an introductory figure. Given the high graphic design quality of the authors other figures, this may be relatively straightforward to add, it will greatly benefit all readers.

In this introductory figure and the associated introductory text, please consider there are numerous well preserved and diverse fossil scorpionflies (e.g. orthophlebiids sensu lato) from the Mesozoic Lagerstätten in China (Middle Jurassic Daohugou Biota, Early Cretaceous Jehol Biota) that are curated across institutions and museums. These collections have been studied in detail. Introducing this fact to the reader and presenting the new fossils in this established context is essential to clearly frame the new findings and show the scientific significance. In this regard the statement "in older fossil panorpoids, the abdomen is lacking or this portion is obscured" should be updated and clarified to avoid overstatement.

2) Regarding the relationship between gift-giving and coercive behavior. Most insects do not have nuptial gifts during the mating, coercive behavior is very common, please integrate this in the framing of Mecoptera as models of evolutionary research. The emergence of nuptial gifts seems to have greatly improved the diversity of reproductive behavior in scorpionflies. Considering this, coercive behavior may perhaps still be considered at the lower level of reproduction. In this light nuptial gifts, rather than coercion, may make scorpionflies an important reproductive evolutionary model. Given the discussion of this matter by the reviewers, it is helpful to clarify the manuscript and either integrate this perspective or provide a compelling rebuttal that the reviewers can evaluate to consider the authors preferred perspective.

3) The abstract could more clearly communicate the key findings and conclusions. Consider further highlighting the new evidence presented for the evolution of reproductive behavior in Mecoptera (/ the Holometabola). Please revise in a fashion that serves the general eLife reader.

4) The introduction should more carefully consider the number of extant species of scorpionflies, which is over 700. Consider that these scorpionflies providing saliva globes typically do not provide the dead arthropods at the same time. This has ramifications for the number of gifts that can be given at one time.

5) The descriptive and Discussion sections should be separated more clearly so the reader can digest the evidence before considering the authors evolutionary interpretation and hypothesis.

6) Present the new family, Cantabridae, in the context of other families of Panorpidea beyond Panorpidae. Consider comparing them further with the Holcorpidae based on their similarity in elongated abdomen. At a higher level, provide higher level context for the general eLife reader so they can follow the merit and relevance of considering the Cantabridae and contrasting them with other families through the lens of evolutionary diversity.

7) The discussion benefits from more clearly structuring the sections with informative subtitles that help the general eLife reader grasp the big picture points. Examples of dry and challenging concepts discussed include, Notal and postnotal organs; Anal horns; Other male abdominal processes; Male abdominal configurations and mating strategies.

8) Please better discuss why there may be both coercive behavior and nuptial gifting in some groups, what's the functional / evolutionary reason? Do more groups have a mixed strategy or only the orthophlebiid? Thoughtful explanation supported by key examples will help clarify this issue in the discussion.

9) Consider that females have several mating options and can choose to accept more than one male, informed by specific behaviors and morphology.

9) Given this study lacks a full-fledged phylogenetic analysis, consider deleting the discussion on phylogenetic relationships. Alternatively, consider providing a phylogenetic analysis of male abdomen morphology to strengthen the rigor of the study. Or if this is infeasible, but the authors wish to make a phylogenetic point, keep in mind that the only acceptable location for speculation is in the last paragraph of the discussion proposing future work in a few concise sentences (at most).

10) The mating behavior of Boreidae scorpionflies is well-described in literature, however, this context is not well-introduced and discussed. E.g. "notal and postnotal organs …can be vestigially present in Boreidae" is technically incorrect. The males of Boreidae have a non-homologous but functionally similar female-clamping device, which include hook-like rudimentary wings and structures on the 2nd and 3rd abdominal segments (vs on 4th and 5th in panorpids), usually referred to as tergal apophyses (e.g. Mickoleit and Mickoleit, 1976), that can be well-developed in some species. However, it is not apparent that this well-developed (better than in most panorpids) clamping device evolved as a male adaptation to sexual conflict over mating duration. Instead, its main function is likely to ease initiation of copulation and to further stabilize the female position throughout mating in order to resist external disturbances (in some species of Boreus, especially European, females usually do not attempt to resist and remain motionless throughout the entire copulation process which may last for hours) (Mickoleit and Mickoleit, 1976; Beutel and Friedrich, 2019). The same may be true for at least some Panorpidae (Kock et al., 2009) so this context may be relevant for extinct scorpionflies too. Please present the new findings in the context of the present literature so that the general eLife reader can easily follow and appreciate the broader context framing the new findings.

11) Please consider for your discussion that Zhang et al., (2021) (DOI: 10.1186/s12862-021-01771-3) reported striking swollen tarsal segments in males of the Middle Jurassic scorpionflies and hypothesized how they may have been associated with nuptial gifting behavior and served to "camouflage a gift in the mating process". These tarsal swellings have been previously known in males of some Late Jurassic Orthophlebiidae (including Orthophlebia longicauda, the one with paired anal horns), and were initially interpreted as possible pheromone glands, tympanal organs (possibly related to premating behavior), or structures for grasping female mates (Novokshonov, 1996; Willmann and Novokschonov, 1998). Either of these assumptions suggests that courtship rituals and nuptial gifting might have already been common among Jurassic scorpionflies. Consider briefly mentioning or discussing this speculative hypothesis so the general reader is aware of the ongoing debate, clarifying how the current fossils relate to the earlier work and may confirm or modify earlier interpretations.

Line items

12) Page 3, Line 16-30: Please clarify the abstract to avoid ambiguity in word meaning / interpretation by the reader. The manuscript should be clear for eLife's broad readership while remaining sufficiently scientifically precise.

13) Page 3, Line 21: Well-preserved fossils are rare, meaningful ones are even more so, consider writing "well-preserved" instead.

14) Page 4, Line 28: Which group, Mecoptera or Panorpoidea, please clarify.

15) Page 4, Line 41-44: please support with references.

16) Page 5, Line 68-71: Revise into shorter clearer sentences. (e.g. we appreciate that: A good correlation has been found in extant panorpids, between their placement of nuptial-coercive mating gradient and morphology of male salivary glands and diverse non-genitalic clamping structures, such as notal-postnotal organs and anal horns. Communicating this clearly is key to engage the reader; revising using shorter sentences helps clarify further)

17) Page 7, Line 109-110: Usually, the name of a family is in Latin or Greek, hence we suggest deleting"-in Spanish.".

18) Page 10, Line 158, 159: Is there a preservation problem? Please better clarify the issue with the forewings.

19) Page 12, Line 210: strongly or reduced?

19) Page 15, Line 236: This manuscript is not about the scientific underpinnings of COVID-19, hence any reference to it has no scientific merit. Please do not name the species after the pandemic and choose a scientifically more appropriate and conventional name instead. (As a side note COVID-19 started in 2019 and not 2020 as stated by the authors: further underscoring the species naming and its motivation can be improved to meet higher scientific standards.)

20) Page 18, Line 297-299: It would help to introduce the explanation earlier at the start of this paragraph.

21) Page 18, Line 307-311: This sentence is too long and unclear.

22) Page 21, Line 366-411: Please simplify this paragraph so it can be understood by the general eLife reader: short and clear sentences that do not overly rely on jargon are optimal.

23) Page 24, Line 418-421: Consider moving this sentence to the beginning of this paragraph and simplify the read for a general reader.

24) Page 25, Line 450-458: There are at least two ways to make a clear comparison: one option is to use a figure that integrates all the information visually side by side; another is to use tables that organize key comparative items in a fashion that makes the comparison comprehensive and intuitive. Or both to more thoroughly substantiate the point.

25) Page 27, Line 503: Please start with a new paragraph. Structuring and organizing the different points in clear paragraphs with a well-defined subject and scope improves the read

26) Page 27, Line 512: To better communicate the evolutionary history, include a timeline in the analysis to frame the corresponding tables / plates to intuitively reflect the evolution process of different taxa and morphology.

27) Figure 1: Please note about 5% of people are color blind, so using red symbols on a green background is confusing at least 5% of the readers. Please improve the color choice, a simple white face color would provide good contrast, also increase symbol size somewhat so it stands out better. Using a white font for "SPAIN" and "MYANMAR" as well as the scale bar will improve readability since black does not have as much contrast with a dark colored background as white.

28) Figure 2: B and G do not have the same color tone as the other photos. Is F enlarged from G? Please help the reader understand and graphically show all relationships when panels represent enlarged sections specifically.

29) Figure 3: are (A) and (B) right or left wings? Please add the anatomical perspective definition for the general reader.

30) Figure 4: (C) and (D), right or left wings?

31) Figure 5: Figure A is this a photo of a complete specimen? Is C an enlarged from B? If so, please mark the specific position.

32) All figures: Please clarify the relationships between panels in figures explicitly in the caption whenever there are relationships such as enlargements, different perspectives, etcetera.

33) Figure 6: Replace "&" with "and" in full text, except references. Also unify NO and PO in the full text.

34) Figure 7: Improve the markup of the male and female in (A).

35) Supplementary Table 1: Change "Figure " to "Figure " throughout. Please add a column to indicate the age and period.

36) References: Please pay attention to the format which should be unified and strictly conform to the requirements of eLife.

37) ln. 181-182: "crossvein present between M4 and Cu1;" Please note that according to Figure 4C and the description (ln. 207), there are two crossveins between M4 and Cu1. Please resolve.

38) ln. 183: "anal veins strongly." is there a word missing? We only see one anal vein on the presented line drawing, are we missing something or is the description incomplete?

39) ln. 205-206: "Rs with five posterior branches; medial sector with five posterior branches"

why posterior? Does that mean there could be any anterior branches as well? Please clarify this matter in the text and response.

40) ln. 209-210: [in hindwing] "anal veins reduced". It seems that A1 is not reduced. Please consider this carefully as well as how reduction may or may not apply elsewhere.

41) ln. 324: "Orthophlebia heidemariae Willmann and Novokshonov, 1988" please correctly refer to "Willmann and Novokshonov, 1998"

42) ln. 418: "Late Jurassic Orthophlebia longicauda (†Orthophlebiidae) from Karatau (Russia)" Please note Karatau Lagerstätte is located in South Kazakhstan, not in Russia

43) ln. 428: "In a Middle Jurassic species, Orthophlebia heidemariae" this is likely erroneous, shouldn't Middle Jurassic be replaced with Late Jurassic?

44) Please consider that Burmophlebia may not be the best name for the new genus, because it sounds very similar to Burmaphlebia by Bechly et Poinar, 2013 (Odonata, Burmaphlebiidae), which will confuse both expert and general readers. Consider Burmorthophlebia as an alternative, or further improve otherwise. A thoughtful improvement would be much appreciated.

45) Please provide relevant measurements for all the morphological descriptions.

46) Regarding "male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa" please consider if the long gonostylus with teeth could function like a weapon or to grasp the female or win a competition among male rivals. E.g. Liu, X., Hayashi, F., Lavine, L. C., and Yang, D. (2015). Is the diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts? Proceedings of the Royal Society B: Biological Sciences, 282(1807), 20150247. In case the authors consider this less relevant, please clarify so the reviewers can fully evaluate the authors perspective. In case the authors see merit in this perspective, please integrate it in a fashion that serves both the general and specialist reader.

47) In Figure 3 regarding the wording "restauration", use "reconstruction".

48) In the first description the justification for a new family name is provided considering differences with the next related family. However, for the other descriptions of Burmophlebia and B. pandemica [please change name] such clarifying context is missing. The differences can be found in the discussion, but systematically including them in a summarized fashion in the descriptive section helps the reader structure the findings.

49) lines 308 and 312 Please specify how long is "short", "medium-size" and "long"? Please provide all key measures explicitly using accepted length scales (SI) as requested in an earlier comment. Then also introduce the relative measures explicitly with length ranges so any reader can follow and understand the point made.

50) In addition to citing Szwedo et al., (2020) consider adding Houg et al., (2020) in case you agree this improves the literature representation. Would it be valuable to include that Haug, J.T., Azar, D., Ross, A. et al., comment on the letter of the Society of Vertebrate Paleontology (SVP) dated April 21, 2020 regarding "Fossils from conflict zones and reproducibility of fossil-based scientific data": Myanmar amber. PalZ 94, 431-437 (2020). https://doi.org/10.1007/s12542-020-00524-9. In case you do not find these citations essential, please briefly explain why so the reviewing editor can judge (eLife does not require additional citations unless they clearly improve the scientific representation of the literature)

51) Consider if this more recent work on Baltic amber age may help the reader frame the current findings: Kasiński, J. R., Kramarska, R., Słodkowska, B., Sivkov, V. and Piwockl, M. Paleocene and Eocene deposits on the eastern margin of the Gulf of Gdańsk (Yantarny P-1 bore hole, Kaliningrad region, Russia). Geol. Q. 64, 20-53 (2020). They concluded the age ranges between ~34 and 38 Ma.Reviewer #1:

This work provides new data for studying the origin and evolution of Panorpidea (Mecoptera), especially important to the exploring of sexual conflict and distinct mating mode. All data provides a critical step and deep-time perspective to illustrate the developmental reasons of gift giving in Mecoptera, and relationship between nuptial gifts and coercive behavior in the most general way.

The paper does have strengths in data, however, these strengths are not well demonstrated. In other words, without insufficiently logical analyses support the key claims, some parts are complex and make it difficult for readers to understand.

In particular:

1) About the relationship between gift-giving and coercive behavior. Most insects do not have nuptial gifts during the mating, coercive behavior is very common, which can not be a reason for Mecoptera to be models of evolutionary research. Practically, the emergence of nuptial gifts greatly improved the diversity of reproductive behavior in scorpionflies, and all different coercive behavior still at the lower level of reproduction. Therefore, nuptial gifts, rather than coercion, is the important reason for scorpionfly become an important reproductive evolutionary model.

2) In Abstract part, the most important points or conclusions are not highlighted, how many mating styles there are not the most important, but new finding provide irreplaceable evidence for the evolution of reproductive behavior in Mecoptera, or even in the Holometabola. In addition, key words should not repeat with the title.

3) In Introduction part, the extant species of scorpionflies is over 700, please pay attention to the numbers. Generally, these scorpionflies that provide the saliva globes do not provide the dead arthropods at the same time, which means usually only offering one gift at one time.

4) In Description part, should not repeat with diagnosis. Remarks of new family (Cantabridae) should compare with other families of Panorpidea, not only the Panorpidae. In addition, better compare with the Holcorpidae, as they have quite similar elongated abdomen.

5) In Discussion part, need to add some subtitles, as this part is quite long, not easy to be logical and clear. For example, Notal and postnotal organs; Anal horns; Other male abdominal processes; Male abdominal configurations and mating strategies. There are both coercive behavior and nuptial gifting in some groups, what's the reason? All groups with weak system have mixed strategy or only orthophlebiid? Need more explanation or examples. Furthermore, females have a great deal of choice in mating, and can choose to accept more than one male, based on specific behaviors and structures. Since this study lack of phylogenetic analysis, better delete the discussion on phylogenetic relationships. Of course, providing a phylogenetic analysis of particular male abdomen structures would greatly enhance the logic and comprehension of this study.Reviewer #2:

The authors describe new interesting scorpionfly fossils preserved in various Cretaceous and Eocene ambers, with a particular focus on certain striking morphological structures that include notal and postnotal organs and other non-genital abdominal processes. Previously, only a few examples of such structures have been known in fossil scorpionflies and they have never been treated in terms of their possible function and role in mating behavior. Based on comparison with various extant panorpid species, the authors speculate about the possible mating strategies in each new taxon under discussion in context of the evolution of mating-related sexual conflict in Mecoptera and insects in general.

The manuscript is well designed, clearly written and well structured, I enjoyed reading it. The discussion is compelling and worth publication. The descriptions of the new taxa are correct, but not without some flaws, which would be easy to fix.

However, there are two important issues that are missing in the manuscript. I think they should be considered before the manuscript is accepted for publication.

1) The mating behavior of Boreidae is not discussed, although it is well-described in literature (the paper is entitled "Evolution of sexual conflict in scorpionflies", and Boreidae are scorpionflies, aren't they?). The only mention of this family is when the authors state that "notal and postnotal organs …can be vestigially present in Boreidae", which is technically incorrect. The males of Boreidae have a non-homologous but functionally similar female-clamping device, which include hook-like rudimentary wings and structures on the 2nd and 3rd abdominal segments (vs on 4th and 5th in panorpids), usually referred to as tergal apophyses (e.g. Mickoleit and Mickoleit, 1976), that can be well-developed in some species. However, it is not apparent that this well-developed (better than in most panorpids) clamping device evolved as a male adaptation to sexual conflict over mating duration. Instead, its main function is likely to ease initiation of copulation and to further stabilize the female position throughout mating in order to resist external disturbances (in some species of Boreus, especially European, females usually do not attempt to resist and remain motionless throughout the entire copulation process which may last for hours) (Mickoleit and Mickoleit, 1976; Beutel and Friedrich, 2019). The same may be true for at least some Panorpidae (Kock et al., 2009), and – who knows? – maybe for some extinct scorpionflies, too.

2) There are hundreds, if not thousands, perfectly preserved and very diverse fossil scorpionflies (mainly orthophlebiids sensu lato) from the famous Mesozoic Lagerstätten in China (Middle Jurassic Daohugou Biota, Early Cretaceous Jehol Biota) available in many institutional and museum collections. I know that some of the authors have extensively studied this material. So, when the authors say that "in older fossil panorpoids, the abdomen is lacking or this portion is obscured", this is not entirely true.

Recently, Zhang et al., (2021) (DOI: 10.1186/s12862-021-01771-3) reported striking swollen tarsal segments in males of the Middle Jurassic scorpionflies and proposed a very interesting hypothesis that those might have been associated with nuptial gifting behavior and served to “camouflage a gift in the mating process”. These tarsal swellings have been previously known in males of some Late Jurassic Orthophlebiidae (including Orthophlebia longicauda, the one with paired anal horns), and were initially interpreted as possible pheromone glands, tympanal organs (possibly related to premating behavior), or structures for grasping female mates (Novokshonov, 1996; Willmann and Novokschonov, 1998). Either of these assumptions suggests that courtship rituals and nuptial gifting might have already been common among Jurassic scorpionflies. As speculative as this hypothesis may be, it should be considered or at least mentioned.Reviewer #3:

Nice and significant contribution about the sexual conflict mating habits of scorpionflies with hifh quality description of three new fossil panorpoid scorpionfly males from different sources of ambers from different ages. The Baltic fossil scorpionflie possesses extreme female clamping abdominal specializations, suggesting the greatest degree of sexual coercion in the group. Based on their different abdominal configurations the fossils show a wide array of mating-related morphological specializations reflecting diversified mating strategies and behaviours.

Reviewer #4:

Soszynska-Maj et al., explain the evolution of sexual conflict by describing three new species of Scorpionflies (Mecoptera) from three different amber resources of different ages and from different geographical areas. Surprising each of the three specimens represent a different mating behavior within the spectrum known nowadays. However, some of the fossil structures used for mating practices are more diverse and specialized, highlighting the importance of the study of fossils. The manuscript is well written and well organized. The data is nicely presented and informative. For non- scorpionflies specialists, the crucial characters are explained, also with the help of figures.

The manuscript focuses on scorpionflies for obvious reasons. First, the three specimens in amber are exceptionally well preserved, and because of their rarity in the fossil record, the specimens are of high scientific value. Second, Mecopterans are used as a model in sexual conflict studies already since many generations. Thus, the opportunity to integrate fossil specimens in such studies is crucial to understand its evolution. I considered the topic highly interesting and important not only for studying the evolution of Mecopterans but also in general for studying the evolution of insects.

Because the topic is treated seldom in the fossil record, the interest in the manuscript for other paleoentomologists would increase with a short paragraph in the introduction that includes other insects that follow similar strategies (Tettigoniidae, Megaloptera) together with some of the most relevant and general references. The species described from the Spanish amber is a new family and comparisons with recent relatives is extreme difficult. May it be necessary to look the strategies of other insects with sexual conflicts.

https://doi.org/10.7554/eLife.70508.sa1

Author response

Essential revisions:

General points

The following revisions improve both the scientific presentation and clarity for eLife's broad readership. Especially considering the paper has strengths in its unique fossil data, however, there is a need to more clearly and logically support the main points informed by the data. Several sections are unnecessary complex, which makes this manuscript unclear for both specialists and general eLife readers alike. Please address the issues thoughtfully and holistically keeping in mind eLife serves the entire biology community by publishing exceptionally clear and rigorously supported manuscripts. Any jargon deemed essential in the manuscript should be introduced in a more accessible fashion upon first use so a general reader can follow.

We have done our best to simplify the Introduction and Discussion parts, either by translating terms or simplifying the text by removing some terms. The discussion is now divided into subsections.

1) Not only the general readership needs improved higher level framing to enable a clear read. Fellow paleoentomologists would also greatly benefit from a paragraph in the introduction that includes other insects that follow similar strategies (e.g. Tettigoniidae, Megaloptera) together with some of the most relevant and general references.

The introduction is enriched by the wider context of mating behaviour, mainly among insects. However, the literature on this subject is so wide that we have limited ourselves to selected examples.

Considering the species found in Spanish amber belong to a new family, it will be challenging to make comparisons with recent relatives.

It is done.

Hence it may serve both the general and specialist reader to present the current findings in the context of mating strategies of other insects with sexual conflicts. To help introduce the general reader to the focus of this study, it would help to present an introductory figure showing this broader context, both in extant and extinct species, highlighting the unique contribution the new fossils make. Optimizing the graphic presentation and introducing key specialist terms in a clear fashion. To find examples for what a general reader would find clear consider how an in-depth National Geographic or New York Times Science article would communicate the context of the new finding and fossil as inspiration for designing an introductory figure. Given the high graphic design quality of the authors other figures, this may be relatively straightforward to add, it will greatly benefit all readers.

We looked at other articles in eLife on similar topics and decided to change the order of figures, to enrich them with clearer elements, such as the whole silhouette of a male and to give a drawing at the beginning to show what the article is about.

In this introductory figure and the associated introductory text, please consider there are numerous well preserved and diverse fossil scorpionflies (e.g. orthophlebiids sensu lato) from the Mesozoic Lagerstätten in China (Middle Jurassic Daohugou Biota, Early Cretaceous Jehol Biota) that are curated across institutions and museums. These collections have been studied in detail. Introducing this fact to the reader and presenting the new fossils in this established context is essential to clearly frame the new findings and show the scientific significance. In this regard the statement "in older fossil panorpoids, the abdomen is lacking or this portion is obscured" should be updated and clarified to avoid overstatement.

Comments on "in older fossil panorpoids, the abdomen is lacking or this portion is obscured": In this sentence about older material we particularly meant the Permian and Triassic Mecoptera. However, due to perhaps too much mental shortcutting, this sentence has been deleted.

2) Regarding the relationship between gift-giving and coercive behavior. Most insects do not have nuptial gifts during the mating, coercive behavior is very common, please integrate this in the framing of Mecoptera as models of evolutionary research. The emergence of nuptial gifts seems to have greatly improved the diversity of reproductive behavior in scorpionflies. Considering this, coercive behavior may perhaps still be considered at the lower level of reproduction. In this light nuptial gifts, rather than coercion, may make scorpionflies an important reproductive evolutionary model. Given the discussion of this matter by the reviewers, it is helpful to clarify the manuscript and either integrate this perspective or provide a compelling rebuttal that the reviewers can evaluate to consider the authors preferred perspective.

Both types of behaviour, a violent behaviour as well as various types of wedding gifts are widespread among animals. A spectrum of examples is now presented in the new introduction. Regarding the question which type was first in Mecoptera (at lower level of reproduction), the data presented here, as well as opinion of other authors (Zhong et al., 2015) suggest rather the reverse, i.e, that plesiomorphic (older, primary) behaviour was rather based on nuptial gifts than on coercion. The impressive armature used by males practising only coercion needed time to evolve. Indeed, is not known in fossil record older than Eocene. We added comment on this to the discussion and the abstract.

3) The abstract could more clearly communicate the key findings and conclusions. Consider further highlighting the new evidence presented for the evolution of reproductive behavior in Mecoptera (/ the Holometabola). Please revise in a fashion that serves the general eLife reader.

It was done.

4) The introduction should more carefully consider the number of extant species of scorpionflies, which is over 700.

Corrected

Consider that these scorpionflies providing saliva globes typically do not provide the dead arthropods at the same time. This has ramifications for the number of gifts that can be given at one time.

We found information that eating dead arthropods by male is necessary to produce salivary gifts, and that the male makes choice: offer a prey, or eat it itself? This would mean that at least some species can both provide either prey, or a salivary glob (Thornhill, 1990) – Introduction 117-119.

5) The descriptive and Discussion sections should be separated more clearly so the reader can digest the evidence before considering the authors evolutionary interpretation and hypothesis.

This is done now.

6) Present the new family, Cantabridae, in the context of other families of Panorpidea beyond Panorpidae. Consider comparing them further with the Holcorpidae based on their similarity in elongated abdomen. At a higher level, provide higher level context for the general eLife reader so they can follow the merit and relevance of considering the Cantabridae and contrasting them with other families through the lens of evolutionary diversity.

The comparison is now included in the remarks to the diagnosis of a new family.

7) The discussion benefits from more clearly structuring the sections with informative subtitles that help the general eLife reader grasp the big picture points. Examples of dry and challenging concepts discussed include, Notal and postnotal organs; Anal horns; Other male abdominal processes; Male abdominal configurations and mating strategies.

The discussion has been divided into parts, subchapters.

8) Please better discuss why there may be both coercive behavior and nuptial gifting in some groups, what's the functional / evolutionary reason? Do more groups have a mixed strategy or only the orthophlebiid? Thoughtful explanation supported by key examples will help clarify this issue in the discussion.

It was added.

9) Consider that females have several mating options and can choose to accept more than one male, informed by specific behaviors and morphology.

This is true, but the research on behaviour of females is based on recent species only, for obvious reasons. Therefore, we focus on the strategies of fossilized males, whose armature stands up the comparison with recent species. However, it is more than possible that is was also females’ response to extreme coercion in Baltipanorpa opressiva and damzeni that resulted in extinction of this genus. The sentence on this is added in the Conclusions, line 515-522. Also in the Introduction, line 96-100 the sentence on female’s response is added.

9) Given this study lacks a full-fledged phylogenetic analysis, consider deleting the discussion on phylogenetic relationships. Alternatively, consider providing a phylogenetic analysis of male abdomen morphology to strengthen the rigor of the study. Or if this is infeasible, but the authors wish to make a phylogenetic point, keep in mind that the only acceptable location for speculation is in the last paragraph of the discussion proposing future work in a few concise sentences (at most).

Considerations of a phylogenetic nature have been removed.

10) The mating behavior of Boreidae scorpionflies is well-described in literature, however, this context is not well-introduced and discussed. E.g. "notal and postnotal organs …can be vestigially present in Boreidae" is technically incorrect. The males of Boreidae have a non-homologous but functionally similar female-clamping device, which include hook-like rudimentary wings and structures on the 2nd and 3rd abdominal segments (vs on 4th and 5th in panorpids), usually referred to as tergal apophyses (e.g. Mickoleit and Mickoleit, 1976), that can be well-developed in some species. However, it is not apparent that this well-developed (better than in most panorpids) clamping device evolved as a male adaptation to sexual conflict over mating duration. Instead, its main function is likely to ease initiation of copulation and to further stabilize the female position throughout mating in order to resist external disturbances (in some species of Boreus, especially European, females usually do not attempt to resist and remain motionless throughout the entire copulation process which may last for hours) (Mickoleit and Mickoleit, 1976; Beutel and Friedrich, 2019).

You are right that, indeed, our bringing up the example of Boreidae here makes no sense, as there are their modified retracted wings which are used to hold the female. The processes on II and III tergites are not holomogous with notal and postnotal organs. After some thought Boreidae were removed from the discussion.

The same may be true for at least some Panorpidae (Kock et al., 2009) so this context may be relevant for extinct scorpionflies too. Please present the new findings in the context of the present literature so that the general eLife reader can easily follow and appreciate the broader context framing the new findings.

It has been added to the discussion.

11) Please consider for your discussion that Zhang et al., (2021) (DOI: 10.1186/s12862-021-01771-3) reported striking swollen tarsal segments in males of the Middle Jurassic scorpionflies and hypothesized how they may have been associated with nuptial gifting behavior and served to “camouflage a gift in the mating process”. These tarsal swellings have been previously known in males of some Late Jurassic Orthophlebiidae (including Orthophlebia longicauda, the one with paired anal horns), and were initially interpreted as possible pheromone glands, tympanal organs (possibly related to premating behavior), or structures for grasping female mates (Novokshonov, 1996; Willmann and Novokschonov, 1998). Either of these assumptions suggests that courtship rituals and nuptial gifting might have already been common among Jurassic scorpionflies. Consider briefly mentioning or discussing this speculative hypothesis so the general reader is aware of the ongoing debate, clarifying how the current fossils relate to the earlier work and may confirm or modify earlier interpretations.

The paper was quoted and the facts added to the discussion. When this paper was sent to eLife, the authors did not yet have access to this paper on leg organs, although the matter is well known to them from their work in Chinese collections.

Line items

12) Page 3, Line 16-30: Please clarify the abstract to avoid ambiguity in word meaning / interpretation by the reader. The manuscript should be clear for eLife’s broad readership while remaining sufficiently scientifically precise.

The Abstract has been changed accordingly.

13) Page 3, Line 21: Well-preserved fossils are rare, meaningful ones are even more so, consider writing “well-preserved” instead.

It has been done.

14) Page 4, Line 28: Which group, Mecoptera or Panorpoidea, please clarify.

It has been done.

15) Page 4, Line 41-44: please support with references.

This sentence is now removed.

16) Page 5, Line 68-71: Revise into shorter clearer sentences. (e.g. we appreciate that: A good correlation has been found in extant panorpids, between their placement of nuptial-coercive mating gradient and morphology of male salivary glands and diverse non-genitalic clamping structures, such as notal-postnotal organs and anal horns. Communicating this clearly is key to engage the reader; revising using shorter sentences helps clarify further)

It has been done.

17) Page 7, Line 109-110: Usually, the name of a family is in Latin or Greek, hence we suggest deleting”-in Spanish.”.

It has been done.

18) Page 10, Line 158, 159: Is there a preservation problem? Please better clarify the issue with the forewings.

Corrected.

19) Page 12, Line 210: strongly or reduced?

Corrected.

19) Page 15, Line 236: This manuscript is not about the scientific underpinnings of COVID-19, hence any reference to it has no scientific merit. Please do not name the species after the pandemic and choose a scientifically more appropriate and conventional name instead. (As a side note COVID-19 started in 2019 and not 2020 as stated by the authors: further underscoring the species naming and its motivation can be improved to meet higher scientific standards.)

Changed.

20) Page 18, Line 297-299: It would help to introduce the explanation earlier at the start of this paragraph.

Corrected.

21) Page 18, Line 307-311: This sentence is too long and unclear.

Corrected.

22) Page 21, Line 366-411: Please simplify this paragraph so it can be understood by the general eLife reader: short and clear sentences that do not overly rely on jargon are optimal.

Corrected.

23) Page 24, Line 418-421: Consider moving this sentence to the beginning of this paragraph and simplify the read for a general reader.

Corrected.

24) Page 25, Line 450-458: There are at least two ways to make a clear comparison: one option is to use a figure that integrates all the information visually side by side; another is to use tables that organize key comparative items in a fashion that makes the comparison comprehensive and intuitive. Or both to more thoroughly substantiate the point.

The illustrations now are changed and supplemented to make them as synthetic as possible, and also the new Table 2 with summary of all fossil armature in males is added in the Supplementary materials.

25) Page 27, Line 503: Please start with a new paragraph. Structuring and organizing the different points in clear paragraphs with a well-defined subject and scope improves the read

Corrected.

26) Page 27, Line 512: To better communicate the evolutionary history, include a timeline in the analysis to frame the corresponding tables / plates to intuitively reflect the evolution process of different taxa and morphology.

An additional figure at the end of the discussion summarising the issue has been added. We hope this will make the article easier to perceive.

27) Figure 1: Please note about 5% of people are color blind, so using red symbols on a green background is confusing at least 5% of the readers. Please improve the color choice, a simple white face color would provide good contrast, also increase symbol size somewhat so it stands out better. Using a white font for “SPAIN” and “MYANMAR” as well as the scale bar will improve readability since black does not have as much contrast with a dark colored background as white.

Corrected.

28) Figure 2: B and G do not have the same color tone as the other photos. Is F enlarged from G? Please help the reader understand and graphically show all relationships when panels represent enlarged sections specifically.

Corrected.

29) Figure 3: are (A) and (B) right or left wings? Please add the anatomical perspective definition for the general reader.

Corrected.

30) Figure 4: (C) and (D), right or left wings?

Corrected.

31) Figure 5: Figure A is this a photo of a complete specimen? Is C an enlarged from B? If so, please mark the specific position.

Corrected.

32) All figures: Please clarify the relationships between panels in figures explicitly in the caption whenever there are relationships such as enlargements, different perspectives, etcetera.

Corrected.

33) Figure 6: Replace "&" with "and" in full text, except references. Also unify NO and PO in the full text.

Corrected.

34) Figure 7: Improve the markup of the male and female in (A).

Corrected.

35) Supplementary Table 1: Change "fig" to "Fig.” throughout. Please add a column to indicate the age and period.

The table refers to recent species; the expression “recent” has been added to the table’s caption.

36) References: Please pay attention to the format which should be unified and strictly conform to the requirements of eLife.

Corrected.

37) ln. 181-182: "crossvein present between M4 and Cu1;" Please note that according to Figure 4C and the description (ln. 207), there are two crossveins between M4 and Cu1. Please resolve.

Corrected.

38) ln. 18“: "anal veins strongly." is there a word missing? We only see one anal vein on the presented line drawing, are we missing something or is the description incomplete?

Corrected.

39) ln. 205-20“: "Rs with five posterior branches; medial sector with five posterior branches" why posterior? Does that mean there could be any anterior branches as well? Please clarify this matter in the text and response.

Corrected.

40) ln. 209-210: [in hindwing] "anal veins reduced". It seems that A1 is not reduced. Please consider this carefully as well as how reduction may or may not apply elsewhere.

Corrected.

41) ln. 32“: "Orthophlebia heidemariae Willmann and Novokshonov, 1988" please correctly refer to "Willmann and Novokshonov, 1998"

Corrected.

42) ln. 41“: "Late Jurassic Orthophlebia longicauda (†Orthophlebiidae) from Karatau (Russia)" Please note Karatau Lagerstätte is located in South Kazakhstan, not in Russia

Corrected.

43) ln. 42“: "In a Middle Jurassic species, Orthophlebia heidemariae" this is likely erroneous, shouldn’t Middle Jurassic be replaced with Late Jurassic?

Corrected.

44) Please consider that Burmophlebia may not be the best name for the new genus, because it sounds very similar to Burmaphlebia by Bechly et Poinar, 2013 (Odonata, Burmaphlebiidae), which will confuse both expert and general readers. Consider Burmorthophlebia as an alternative, or further improve otherwise. A thoughtful improvement would be much appreciated.

Thank you for this remark. Corrected.

45) Please provide relevant measurements for all the morphological descriptions.

Corrected in places where it was possible.

46) Regarding "male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa" please consider if the long gonostylus with teeth could function like a weapon or to grasp the female or win a competition among male rivals. E.g. Liu, X., Hayashi, F., Lavine, L. C., and Yang, D. (2015). Is the diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts? Proceedings of the Royal Society B: Biological Sciences, 282(1807), 20150247. In case the authors consider this less relevant, please clarify so the reviewers can fully evaluate the authors perspective. In case the authors see merit in this perspective, please integrate it in a fashion that serves both the general and specialist reader.

The paper you refer to deals with Corydalidae (Megaloptera), and is known to us and cited in our paper several times. The trade-off game between weapons and nuptial gifts also occurs in Mecoptera, of course, and we refer in the revised version to this game and its role for evolution of the group in the introduction and in the discussion.

47) In Figure 3 regarding the wording "restoration", use "reconstruction".

Corrected.

48) In the first description the justification for a new family name is provided considering differences with the next related family. However, for the other descriptions of Burmophlebia and B. pandemica [please change name] such clarifying context is missing. The differences can be found in the discussion, but systematicallyincluding them in a summarized fashion in the descriptive section helps the reader structure the findings.

The name “pandemica” is changed to “opressiva”.

Differentiating diagnosis for Burmorthophlebia and Baltipanorpa opressiva are provided, as well as remarks for Burmorthophlebia.

49) lines 308 and 312 Please specify how long is "short“, "medium-size" and "long"? Please provide all key measures explicitly using accepted length scales (SI) as requested in an earlier comment. Then also introduce the relative measures explicitly with length ranges so any reader can follow and understand the point made.

Explanations have been added to the text.

50) In addition to citing Szwedo et al., (2020) consider adding Houg et al., (2020) in case you agree this improves the literature representation. Would it be valuable to include that Haug, J.T., Azar, D., Ross, A. et al., comment on the letter of the Society of Vertebrate Paleontology (SVP) dated April 21, 2020 regarding “Fossils from conflict zones and reproducibility of fossil-based scientific data”: Myanmar amber. PalZ 94, 431-437 (2020). https://doi.org/10.1007/s12542-020-00524-9. In case you do not find these citations essential, please briefly explain why so the reviewing editor can judge (eLife does not require additional citations unless they clearly improve the scientific representation of the literature)

Paper has been added.

51) Consider if this more recent work on Baltic amber age may help the reader frame the current findings: Kasiński, J. R., Kramarska, R., Słodkowska, B., Sivkov, V. and Piwockl, M. Paleocene and Eocene deposits on the eastern margin of the Gulf of Gdańsk (Yantarny P-1 bore hole, Kaliningrad region, Russia). Geol. Q. 64, 20-53 (2020). They concluded the age ranges between ~34 and 38 Ma.

Corrected.

https://doi.org/10.7554/eLife.70508.sa2

Article and author information

Author details

  1. Agnieszka Soszyńska-Maj

    Faculty of Biology and Environmental Protection, Department of Invertebrate Zoology and Hydrobiology, University of Łódź, Łódź, Poland
    Contribution
    Conceptualization, Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft, Writing – review and editing
    For correspondence
    agnieszka.soszynska@biol.uni.lodz.pl
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2661-6685
  2. Ewa Krzemińska

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland
    Contribution
    Conceptualization, Validation, Visualization, Writing – original draft, Writing – review and editing
    For correspondence
    ekrzeminska9@gmail.com
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3431-9963
  3. Ricardo Pérez-de la Fuente

    Oxford University Museum of Natural History, Oxford, United Kingdom
    Contribution
    Conceptualization, Investigation, Resources, Validation, Visualization, Writing – original draft, Writing – review and editing
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2830-2639
  4. Ji-Shen Wang

    College of Agriculture and Biological Sciences, Dali University, Dali, China
    Contribution
    Investigation, Methodology, Resources, Validation, Visualization
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0188-0228
  5. Krzysztof Szpila

    Department of Ecology and Biogeography, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus University, Toruń, Poland
    Contribution
    Conceptualization, Validation, Writing – original draft, Writing – review and editing
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3039-3146
  6. Kornelia Skibińska

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland
    Contribution
    Investigation, Software, Validation, Visualization
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5971-9373
  7. Katarzyna Kopeć

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland
    Contribution
    Data curation, Investigation, Project administration, Resources, Validation
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6449-3412
  8. Wiesław Krzemiński

    Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland
    Contribution
    Conceptualization, Funding acquisition, Investigation, Resources, Supervision, Validation, Writing – original draft, Writing – review and editing
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5685-891X

Funding

National Science Centre, Poland (2013/09/B/NZ8/03270)

  • Agnieszka Soszyńska-Maj
  • Katarzyna Kopeć
  • Wiesław Krzemiński

National Science Centre, Poland (2016/23/B/NZ8/00936)

  • Agnieszka Soszyńska-Maj
  • Ewa Krzemińska
  • Kornelia Skibińska
  • Katarzyna Kopeć
  • Wiesław Krzemiński

AEI/FEDER, UE (CGL2017-84419)

  • Ricardo Pérez-de la Fuente

Dali University (High-level Talents KY2096124040)

  • Ji-Shen Wang

National Science Centre, Poland (2018/31/B/NZ8/02113)

  • Krzysztof Szpila

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

We express our gratitude to the Editor and four Reviewers for the extensive comments. We thank the El Soplao Cave for providing access to the Spanish amber specimen. Drs Enrique Peñalver and Xavier Delclòs are thanked for managing the loan of that specimen and providing support and discussions, and Rafael López del Valle for its preparation. Sigitas Podenas is thanked for the gift of specimens of Panorpa amuriensis.

Senior Editor

  1. Molly Przeworski, Columbia University, United States

Reviewing Editor

  1. David Lentink, University of Groningen, Netherlands

Reviewers

  1. Ren Dong
  2. Alexei Bashkuev
  3. Dany Azar

Publication history

  1. Received: May 18, 2021
  2. Accepted: February 10, 2022
  3. Accepted Manuscript published: February 11, 2022 (version 1)
  4. Version of Record published: April 5, 2022 (version 2)

Copyright

© 2022, Soszyńska-Maj et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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  1. Agnieszka Soszyńska-Maj
  2. Ewa Krzemińska
  3. Ricardo Pérez-de la Fuente
  4. Ji-Shen Wang
  5. Krzysztof Szpila
  6. Kornelia Skibińska
  7. Katarzyna Kopeć
  8. Wiesław Krzemiński
(2022)
Evolution of sexual conflict in scorpionflies
eLife 11:e70508.
https://doi.org/10.7554/eLife.70508
  1. Further reading

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